MicroRNA-1 regulates chondrocyte phenotype by repressing histone deacetylase 4 during growth plate development

FASEB J. 2014 Sep;28(9):3930-41. doi: 10.1096/fj.13-249318. Epub 2014 May 23.

Abstract

MicroRNAs (miRs) are noncoding RNAs (17-25 nt) that control translation and/or mRNA degradation. Using Northern blot analysis, we identified that miR-1 is specifically expressed in growth plate cartilage in addition to muscle tissue, but not in brain, intestine, liver, or lung. We obtained the first evidence that miR-1 is highly expressed in the hypertrophic zone of the growth plate, with an 8-fold increase compared with the proliferation zone; this location coincides with the Ihh and Col X expression regions in vivo. MiR-1 significantly induces chondrocyte proliferation and differentiation. We further identified histone deacetylase 4 (HDAC4) as a target of miR-1. HDAC4 negatively regulates chondrocyte hypertrophy by inhibiting Runx2, a critical transcription factor for chondrocyte hypertrophy. MiR-1 inhibits both endogenous HDAC4 protein by 2.2-fold and the activity of a reporter gene bearing the 3'-untranslated region (UTR) of HDAC4 by 3.3-fold. Conversely, knockdown of endogenous miR-1 relieves the repression of HDAC4. Deletion of the miR-1 binding site in HDAC4 3'-UTR or mutated miR-1 abolishes miR-1-mediated inhibition of the reporter gene activity. Overexpression of HDAC4 reverses miR-1 induction of chondrocyte differentiation markers Col X and Ihh. HDAC4 inhibits Runx2 promoter activity in a dosage-dependent manner. Thus, miR-1 plays an important role in the regulation of the chondrocyte phenotype during the growth plate development via direct targeting of HDAC4.

Keywords: HDAC4; Runx2; collagen X; differentiation.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Blotting, Northern
  • Blotting, Western
  • Cell Proliferation
  • Cells, Cultured
  • Chick Embryo
  • Chondrocytes / cytology*
  • Chondrocytes / metabolism
  • Chondrogenesis / physiology*
  • Collagen Type X / genetics
  • Collagen Type X / metabolism
  • Core Binding Factor Alpha 1 Subunit / genetics*
  • Core Binding Factor Alpha 1 Subunit / metabolism
  • Flow Cytometry
  • Gene Expression Regulation*
  • Growth Plate / cytology*
  • Growth Plate / metabolism
  • Hedgehog Proteins / genetics
  • Hedgehog Proteins / metabolism
  • Histone Deacetylases / genetics
  • Histone Deacetylases / metabolism*
  • Humans
  • In Situ Hybridization
  • Luciferases / metabolism
  • MicroRNAs / genetics*
  • Promoter Regions, Genetic / genetics
  • RNA, Messenger / genetics
  • Real-Time Polymerase Chain Reaction
  • Repressor Proteins / genetics
  • Repressor Proteins / metabolism*
  • Reverse Transcriptase Polymerase Chain Reaction

Substances

  • Collagen Type X
  • Core Binding Factor Alpha 1 Subunit
  • Hedgehog Proteins
  • IHH protein, human
  • MIRN1 microRNA, human
  • MicroRNAs
  • RNA, Messenger
  • RUNX2 protein, human
  • Repressor Proteins
  • Luciferases
  • HDAC4 protein, human
  • Histone Deacetylases